Abstract
Potato (Solanum tuberosum) and tomato (Solanum lycopersicon) crops suffer severe losses to late blight caused by the oomycete pathogen Phytophthora infestans. Solanum americanum, a relative of potato and tomato, is globally distributed and most accessions are highly blight resistant. We generated high-quality reference genomes of four S. americanum accessions, resequenced 52 accessions, and defined a pan-NLRome of S. americanum immune receptor genes. We further screened for variation in recognition of 315P. infestans RXLR effectors in 52 S. americanum accessions. Using these genomic and phenotypic data, we cloned three NLR-encoding genes, Rpi-amr4, R02860 and R04373, that recognize cognate P. infestans RXLR effectors PITG_22825 (AVRamr4), PITG_02860 and PITG_04373. These genomic resources and methodologies will support efforts to engineer potatoes with durable late blight resistance and can be applied to diseases of other crops.
| Original language | English |
|---|---|
| Pages (from-to) | 1579-1588 |
| Number of pages | 10 |
| Journal | Nature Genetics |
| Volume | 55 |
| Issue number | 9 |
| Early online date | 28 Aug 2023 |
| DOIs | |
| Publication status | Published - Sept 2023 |
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In: Nature Genetics, Vol. 55, No. 9, 09.2023, p. 1579-1588.
Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - Solanum americanum genome-assisted discovery of immune receptors that detect potato late blight pathogen effectors
AU - Lin, Xiao
AU - Jia, Yuxin
AU - Heal, Robert
AU - Prokchorchik, Maxim
AU - Sindalovskaya, Maria
AU - Olave-Achury, Andrea
AU - Makechemu, Moffat
AU - Fairhead, Sebastian
AU - Noureen, Azka
AU - Heo, Jung
AU - Witek, Kamil
AU - Smoker, Matthew
AU - Taylor, Jodie
AU - Shrestha, Ram-Krishna
AU - Lee, Yoonyoung
AU - Zhang, Chunzhi
AU - Park, Soon Ju
AU - Sohn, Kee Hoon
AU - Huang, Sanwen
AU - Jones, Jonathan D. G.
N1 - Data availability statement: The raw sequencing data and genome assemblies of SP1102, SP2271, SP2273 and SP2275 genomes have been deposited at the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) with BioProject accession number PRJNA845062; The raw SMRT RenSeq data were deposited in ENA under project number PRJEB38240. The whole-genome resequencing data were deposited in ENA under project number PRJEB57057. The BSA-RenSeq data were deposited in ENA under project numbers PRJEB57070 and PRJEB57074. The assembled genomes, gene structure annotations, SMRT-RenSeq assemblies and manually annotated NLR genes as well as variation information are available at Figshare (https://figshare.com/projects/The_Solanum_americanum_pangenome_and_effectoromics_reveals_new_resistance_genes_against_potato_late_blight/145449). The SaNRC1-1102, SaNRC2-1102, SaNRC3-1102, Rpi-amr4-1102, Rpi-amr4-2271, R02860 (Rpi-amr16) and R04373 (Rpi-amr17) sequences were deposited at NCBI GenBank under accession number OP918030–OP918036. Source data are provided with this paper. Code availability: Custom scripts and codes used in this study are available at Zenodo (https://doi.org/10.5281/zenodo.7928678). Funding Information: This research was financed by BBSRC grants BB/P021646/1 (J.D.G.J.), BB/S018832/1 (J.D.G.J.), BB/W017423/1 (J.D.G.J.), the Gatsby Charitable Foundation (J.D.G.J.), National Key Research and Development Program of China (2019YFA0906200, S.H.), Guangdong Major Project of Basic and Applied Basic Research (2021B0301030004, S.H.), Agricultural Science and Technology Innovation Program (CAAS-ZDRW202101, S.H.), Shenzhen Outstanding Talents Training Fund (S.H.), National Research Foundation of Korea (2018R1A5A1023599 and 2023R1A2C3002366, K.H.S.) and New Breeding Technologies Development Program (PJ015799 and PJ016538, S.J.P.). We thank TSL transformation team (A. Wawryk-Khamdavong), SynBio team (M. Youles and L. Egan), media services (N. Stammars), bioinformatics team (D. MacLean and C. Jégousse) and horticultural team (S. Perkins, J. Smith, L. Phillips, C. Taylor, T. Wells, D. Alger and S. Able) for their support. We thank P. Robinson (JIC) for the scientific photography. We thank S. Marillonnet (Icon Genetics GmbH, Halle/Saale, Germany) for sharing the Cas9 construct (pAGM47523). We thank Experimental Garden and Genebank of Radboud University, Nijmegen, the Netherlands, IPK Gatersleben, Germany and S. Knapp (Natural History Museum, London, UK) for access to S. americanum genetic diversity. We thank V. G. A. A. Vleeshouwers at Wageningen University and Research, P. Birch, I. Hein and B. Harrower at James Hutton Institute for making available clones of some effectors. We thank B. B.H. Wulff, S. Arora and K. Gaurav (JIC) for helpful discussions. Funding Information: This research was financed by BBSRC grants BB/P021646/1 (J.D.G.J.), BB/S018832/1 (J.D.G.J.), BB/W017423/1 (J.D.G.J.), the Gatsby Charitable Foundation (J.D.G.J.), National Key Research and Development Program of China (2019YFA0906200, S.H.), Guangdong Major Project of Basic and Applied Basic Research (2021B0301030004, S.H.), Agricultural Science and Technology Innovation Program (CAAS-ZDRW202101, S.H.), Shenzhen Outstanding Talents Training Fund (S.H.), National Research Foundation of Korea (2018R1A5A1023599 and 2023R1A2C3002366, K.H.S.) and New Breeding Technologies Development Program (PJ015799 and PJ016538, S.J.P.). We thank TSL transformation team (A. Wawryk-Khamdavong), SynBio team (M. Youles and L. Egan), media services (N. Stammars), bioinformatics team (D. MacLean and C. Jégousse) and horticultural team (S. Perkins, J. Smith, L. Phillips, C. Taylor, T. Wells, D. Alger and S. Able) for their support. We thank P. Robinson (JIC) for the scientific photography. We thank S. Marillonnet (Icon Genetics GmbH, Halle/Saale, Germany) for sharing the Cas9 construct (pAGM47523). We thank Experimental Garden and Genebank of Radboud University, Nijmegen, the Netherlands, IPK Gatersleben, Germany and S. Knapp (Natural History Museum, London, UK) for access to S. americanum genetic diversity. We thank V. G. A. A. Vleeshouwers at Wageningen University and Research, P. Birch, I. Hein and B. Harrower at James Hutton Institute for making available clones of some effectors. We thank B. B.H. Wulff, S. Arora and K. Gaurav (JIC) for helpful discussions.
PY - 2023/9
Y1 - 2023/9
N2 - Potato (Solanum tuberosum) and tomato (Solanum lycopersicon) crops suffer severe losses to late blight caused by the oomycete pathogen Phytophthora infestans. Solanum americanum, a relative of potato and tomato, is globally distributed and most accessions are highly blight resistant. We generated high-quality reference genomes of four S. americanum accessions, resequenced 52 accessions, and defined a pan-NLRome of S. americanum immune receptor genes. We further screened for variation in recognition of 315P. infestans RXLR effectors in 52 S. americanum accessions. Using these genomic and phenotypic data, we cloned three NLR-encoding genes, Rpi-amr4, R02860 and R04373, that recognize cognate P. infestans RXLR effectors PITG_22825 (AVRamr4), PITG_02860 and PITG_04373. These genomic resources and methodologies will support efforts to engineer potatoes with durable late blight resistance and can be applied to diseases of other crops.
AB - Potato (Solanum tuberosum) and tomato (Solanum lycopersicon) crops suffer severe losses to late blight caused by the oomycete pathogen Phytophthora infestans. Solanum americanum, a relative of potato and tomato, is globally distributed and most accessions are highly blight resistant. We generated high-quality reference genomes of four S. americanum accessions, resequenced 52 accessions, and defined a pan-NLRome of S. americanum immune receptor genes. We further screened for variation in recognition of 315P. infestans RXLR effectors in 52 S. americanum accessions. Using these genomic and phenotypic data, we cloned three NLR-encoding genes, Rpi-amr4, R02860 and R04373, that recognize cognate P. infestans RXLR effectors PITG_22825 (AVRamr4), PITG_02860 and PITG_04373. These genomic resources and methodologies will support efforts to engineer potatoes with durable late blight resistance and can be applied to diseases of other crops.
UR - https://www.scopus.com/pages/publications/85168855822
U2 - 10.1038/s41588-023-01486-9
DO - 10.1038/s41588-023-01486-9
M3 - Article
C2 - 37640880
AN - SCOPUS:85168855822
SN - 1061-4036
VL - 55
SP - 1579
EP - 1588
JO - Nature Genetics
JF - Nature Genetics
IS - 9
ER -